Ryals Dylan K, Buschkoetter Amos C, Given J Krispn, Harpur Brock A
Department of Entomology, Purdue University, 901 Mitch Daniels Blvd., West Lafayette, IN 47907, United States.
J Hered. 2025 Jan 3;116(1):54-61. doi: 10.1093/jhered/esae043.
Heterosis occurs in individuals when genetic diversity, e.g., heterozygosity, increases fitness. Many advanced eusocial insects evolved mating behaviors, including polyandry and polygyny, which increase inter-individual genetic diversity within colonies. The possibility of this structure of diversity to improve group fitness has been termed social heterosis. Neither the independence of individual and social heterosis nor their relative effect sizes have been explicitly measured. Through controlled breeding between pairs of Western honey bee queens (Apis mellifera L.; n = 3 pairs) from two distinct populations, we created inbred colonies with low genetic diversity, hybrid colonies with high heterozygosity, and mixed colonies (combining inbred workers from each population) with low heterozygosity and high social diversity. We then quantified two independent traits in colonies: survival against bacterial challenge and maintenance of brood nest temperature. For both traits, we found hybrid and mixed colonies outperformed inbred colonies but did not perform differently from each other. During immune challenge assays, hybrid and mixed colonies experienced hazard ratios of 0.49 (95% CI [0.37, 0.65]) and 0.69 (95% CI [0.50, 0.96]) compared to inbred colonies. For nest temperatures, hybrid and mixed colonies experienced 1.94 ± 0.97 °C and 2.82 ± 2.46 °C less thermal error and 0.14 ± 0.11 °C2 and 0.16 ± 0.06 °C2 less thermal variance per hour than inbred lines. This suggests social and individual heterosis operate independently and may have similar effect sizes. These results highlight the importance of both inter- and intra-individual diversity to fitness, which may help explain the emergence of polyandry/polygyny in eusocial insects and inform breeding efforts in these systems.
当遗传多样性（例如杂合性）提高适应性时，杂种优势就会在个体中出现。许多高等群居昆虫进化出了交配行为，包括一妻多夫制和一夫多妻制，这些行为增加了群体内个体间的遗传多样性。这种多样性结构提高群体适应性的可能性被称为社会杂种优势。个体杂种优势和社会杂种优势的独立性及其相对效应大小均未得到明确测量。通过对来自两个不同种群的西方蜜蜂蜂后（意大利蜜蜂；n = 3对）进行成对控制育种，我们创建了遗传多样性低的近交群体、杂合度高的杂交群体以及杂合度低但社会多样性高的混合群体（将每个种群的近交工蜂组合在一起）。然后，我们对群体中的两个独立性状进行了量化：抵抗细菌攻击的能力和育雏巢温度的维持。对于这两个性状，我们发现杂交群体和混合群体的表现均优于近交群体，但它们之间的表现没有差异。在免疫挑战试验中，与近交群体相比，杂交群体和混合群体的风险比分别为0.49（95%置信区间[0.37, 0.65]）和0.69（95%置信区间[0.50, 0.96]）。对于巢温，杂交群体和混合群体每小时的热误差分别比近交系少1.94±0.97℃和2.82±2.46℃，热方差分别比近交系少0.14±0.11℃²和0.16±0.06℃²。这表明社会杂种优势和个体杂种优势独立起作用，且可能具有相似的效应大小。这些结果突出了个体间和个体内多样性对适应性的重要性，这可能有助于解释群居昆虫中一妻多夫制/一夫多妻制的出现，并为这些系统中的育种工作提供参考。
